In the eastern tropical Pacific (ETP), large mixed-species aggregations of dolphins, tunas, and seabirdsare common. Central to these aggregations are pan -tropical spotted dolphins Stenella attenuata and yellowfin tuna Thunnus albacares. Tuna fishermenhave exploited this association for many decadesbecause the dolphins are easier to sight at a distanceand make the tuna swimming beneath them easier tofollow and catch. In the years following World War II,baitboat fishermen would sight dolphin herds, cued
often by the presence of seabirds overhead, and thenchum the water with live baitfish to attract tuna to thesurface and catch them with hook-and-line gear. Bythe mid 1960s, however, the baitboat fishery hadlargely been transformed into a purse-seine fishery,and the dolphins were no longer used just to find thetuna, but were actively chased and encircled to catchthe tuna (Perrin 1968, Green et al. 1972). Despite thelong history of fishing tunas associated with dolphinsand the intensive management-oriented researchon the 2 species, there are still questions about thebiological basis for the association.
ABSTRACT: The association of yellowfin tuna and pantropical spotted dolphins in the easterntropical Pacific Ocean (ETP) has been exploited by tuna fishermen and has intrigued scientists fordecades, yet we still have questions about what the benefits of the association are—whether theassociation is obligatory or facultative, why the tuna are most often found with spotted dolphins,and why the species associate most strongly in the ETP. We review the hypotheses that have beenproposed to explain the bond and present results from 3 studies conducted to address thesehypotheses: a simultaneous tracking study of spotted dolphins and yellowfin tuna, a trophic inter-actions study comparing their prey and daily foraging patterns, and a spatial study of oceano-graphic features correlated with the tuna–dolphin association. These studies demonstrate that theassociation is neither permanent nor obligatory and that the benefits of the association are notbased on feeding advantages. These studies do support the hypothesis that one or both speciesreduce the risk of predation by forming large, mixed-species groups. The association is mostprevalent where the habitat of the tuna is compressed to the warm, shallow, surface waters of themixed layer by the oxygen minimum zone, a thick layer of oxygen-poor waters underlying themixed layer. The association has been observed in other oceans with similar oceanographic con-ditions, but it is most prevalent and consistent in the ETP, where the oxygen minimum zone is themost hypoxic and extensive in the world.
Michael D. Scott1,*, Susan J. Chivers2, Robert J. Olson1, Paul C. Fiedler2, Kim Holland3
1Inter-American Tropical Tuna Commission, 8604 La Jolla Shores Dr., La Jolla California 92037, USA2Protected Resources Division, Southwest Fisheries Science Center, National Marine Fisheries Service, NOAA,
3333 North Torrey Pines Court, La Jolla, California 92037, USA3Hawaii Institute of Marine Biology, University of Hawaii at Manoa, PO Box 1346, Coconut Island, Kaneohe, Hawaii 96744, USA
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This paper reviews what is known about the asso-ciation and the hypotheses that have been proposedto explain the association, and presents results from 3studies that could support or contradict these hypo -theses. We know that the association between tunaand dolphins is much more prevalent in the ETP thanin other oceans (Joseph & Greenough 1979, Scott etal. 1999). Early oceanographic studies recognizedseveral distinctive features of the ETP: warm surfacewaters, a shallow thermocline (usually less than 60 mdeep), and a thick oxygen minimum zone just belowthe thermocline (Wyrtki 1964, reviews by Fiedler &Lavín 2006, Fiedler & Talley 2006). These featureshave been thought to enhance fishing success by lim-iting the vertical distribution of the yellowfin tuna tothe warm mixed layer near the surface (Green 1967)and promoting the tuna–dolphin association (Perrinet al. 1973, 1976, Au & Perryman 1985). Fishermenwere quick to determine that tuna were found mostreliably with spotted dolphins, although they werealso sometimes caught with other dolphin speciessuch as spinner dolphins Stenella longirostris andshort-beaked common dolphins Delphinus delphis.
Yellowfin and skipjack Katsuwonus pelamis tunasare schooling species that are frequently found inlarge aggregations and we know that the tuna–dolphin association is one of 3 modes of tuna aggre-gation in the ETP. Aggregations of the smaller yel-lowfin, skipjack and bigeye tuna (‘logfish’) are alsocommonly found in association with natural floatingobjects such as logs or with manmade fish aggregat-ing devices (FADs) seeded by the fishermen to catchtunas more efficiently. In addition, tuna aggregationsare often found as free-swimming schools (‘school -fish’) that are not associated with either dolphins orfloating objects. Purse-seine fisheries around theworld typically catch schoolfish and logfish, but in theETP, catching tuna associated with dolphins is com-mon, and it has been suggested that the tuna–dolphinassociation may be an extension of the tendency ofsmall tuna to associate with floating objects (Hall etal. 1999). The association with dolphins occurs whenthe yellowfin tuna become large enough to keep pacewith the more mobile dolphins (Edwards 1992).
A number of hypotheses have been suggested toex plain why tuna and dolphins associate (see re viewsby Hammond 1981, Stuntz 1981, Allen 1985, Fréon& Misund 1999, Fréon & Dagorn 2000). After manyyears of observation and research, however, 2 mainhypotheses have emerged to explain the association:(1) one or both species may gain direct or indirect foraging benefits from the association, and (2) one orboth species may reduce their risk of predation.
Foraging benefits
One potential benefit of the association is that itimproves foraging success. One or both species maybenefit because their large moving aggregation mayflush prey (such as flyingfish), tuna may benefit fromthe dolphins’ ability to echolocate prey at a distance,while dolphins may benefit from the tuna’s superiorsense of smell (Norris 1978, Norris & Dohl 1980a,Au 1991, Pryor & Kang-Schallenberger 1991, Edwards1992, Norris et al. 1994). The association occurswhere the thermocline is shallow (Au & Pitman 1986,Edwards 1992, Norris et al. 1994, Hall et al. 1999),and an energetics model (Edwards 1992) predictsthat the association, if based on feeding, would mostlikely occur where prey is distributed in rare, butrich, patches. The association may be involuntary forthe dolphins because large tuna can swim faster thanthe dolphins (Pryor & Kang-Schallenberger 1991,Edwards 1992).
Temporary feeding aggregations on a commonprey by tunas and dolphins have been observedin other waters. Near the Azores, large yellowfinand bluefin Thunnus thynnus tunas (>100 kg) arethought to gain advantages when feeding with com-mon dolphins Delphinus spp. and Atlantic spotteddolphins Stenella frontalis (Clua & Grosvalet 2001).The dolphins foraged by herding prey fishes into atight ball near the surface, but the tunas tended tobreak up the ball, scattering both prey and dolphins.Groups of yellowfin tuna and spinner dolphins alsohave been observed foraging together off Brazil (Saz-ima et al. 2006). In neither of these areas, however,have the tunas and dolphins been observed in morethan temporary feeding aggregations.
An alternative idea, that dolphins may gain feed-ing advantages by associating with the tuna was pro-posed by Au & Pitman (1986, 1988). Tunas are knownto drive prey to the surface and many seabirds arestrongly dependent on this source of prey (Ashmole& Ashmole 1967). The feeding advantages that sea -birds gain from associating with the tuna, it is argued,could be gained by the dolphins as well.
Protection from predators
One benefit of travelling in large groups of fish ormammals is to reduce an individual’s risk of pre -dation (see reviews by Brock & Riffenburgh 1960,Hamilton 1971, Jarman 1974, Partridge 1982, Inman& Krebs 1987). Reduced risk may be due to the dilu-tion effect (whereby the risk is lessened by spreading
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it over a larger number of individuals), the confusioneffect (whereby predators have increased difficultyin tracking a potential target within a large group ofsimilarly colored and rapidly moving individuals),the encounter effect (whereby a single predatorwould be less likely to encounter prey that is concen-trated in a few large groups rather than dispersed inmany smaller groups), and the vigilance effect(whereby predators can be detected more readily byintegrating the senses of a large number of indi -viduals). Large sharks and billfishes are commonlycaught in association with tunas in the ETP (Au 1991,Hunsicker et al. 2012), and are known both to preyon tunas and dolphins and to compete with them forthe same prey (Leatherwood et al. 1973, Scott & Cattanach 1998, Galván-Magaña 1999, Heithaus2001, Acevedo-Gutiérrez 2002, Maldini 2003, Santos-Monteiro et al. 2006, Bocanegra-Castillo 2007, Fe -lando & Medina 2011, Hunsicker et al. 2012). Falsekiller whales Pseudorca crassidens and killer whalesOrcinus orca are also known predators (Perrin &Hohn 1994, Pitman et al. 2003). Au et al. (1999) notedthat yellowfin tuna would stop feeding to follow spot-ted dolphins that were attempting to avoid theirresearch ship and suggested that ‘fleeing with dol-phins would be advantageous to tuna if, as a generaltactic, it results in escaping predators most of thetime’. Scott & Cattanach (1998) argued that, becausespotted dolphins and yellowfin tuna have many ofthe same potential predators, dolphin herds in theETP increase during the daytime to reduce the riskof predation, and schools of large yellowfin tunaincrease as well due to their association with the dolphins.
Exploring the hypotheses
We conducted 3 studies in the ETP to provide infor-mation that could support or contradict these hypo -theses. The first was a simultaneous tracking studythat used pressure-sensitive sonic transmitters ontuna and radiotags and time-depth recorders (TDRs)on dolphins to record movements and diving pat-terns. The second was a trophic interactions studythat examined the stomach contents of dolphins andtunas captured together in purse-seine nets. Thethird used information collected by observers aboardtuna purse seiners on the spatial extent of the tuna–dolphin association in relation to oceanographic features. The results from these and previous stud-ies could answer pivotal questions about the tuna–dolphin association: whether the association is oblig-
atory for either species, which species initiates theassociation, what the benefits of the association arefor one or both species, why the association primarilyoccurs between large yellowfin and spotted dolphins,and why the species associate so strongly in the ETPand not elsewhere.
SIMULTANEOUS TRACKING
Methods
The simultaneous tracking study was conductedduring a 30 day research cruise in November toDecember 1993 aboard the NOAA RV ‘McArthur’and the chartered purse seiner ‘Convemar’. Details ofthe capture, tagging, and tracking of the dolphins aredescribed by Scott & Chivers (2009). In summary,tuna–dolphin aggregations were encircled by thepurse seiner. The dolphins were caught by swimmersinside the net, placed in a raft, outfitted with radiotransmitters, and released back inside the net so thatthe entire aggregation could be released from the nettogether. Transmitters were mounted on plastic sad-dles that were attached to the dorsal fin with Delrinpins secured by corrodible magnesium nuts; TDRswere also incorporated into most of the dolphin trans-mitter packages. TDRs recorded the time and thedepth of the package every 5 s, and the data wererecovered when the dolphin was recaptured and thepackage removed.
The tuna were tagged with sonic transmitters at-tached to flat dart heads. Three types of trans mitterswere used: one type gave only horizontal movementinformation (Model V3: 71 kHz, range 0.5−0.75 nauti-cal miles (n miles), VEMCO), while the other 2 alsotransmitted the ambient pressure to monitor the ani -mals’ swimming depth (Models V7P: 50 kHz, range0.75− 1.0 n miles, and V3P: 60 kHz, range 0.5−0.75 nmiles, VEMCO). The transmitters had no minal longe -vities of 8 to 13 days. Swimmers used lances to im-plant the dart tips into the dorsal musculature of theyellowfin tuna as they were being released from thenet. We attempted to tag 2 tuna per set, a primary fo-cal animal with the longer range V7P tag, and abackup animal in case the primary animal could notbe released. We attempted to release all the dolphinsand tuna together, either by the normal backdown re-lease procedure (Coe & Sousa 1972) or by releasingone end of the net (‘dropping the ortza’) from theboat, creating an opening for the animals to escape.
Two tracking boats (5 to 9 m long) were riggedwith sonic- and radio-tracking gear to track both
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dolphins and tuna. A receiver and hydrophone(Models VR-60 receiver and VH-65 hydrophone,VEMCO) were mounted on the tracking boats usinga system described by Holland et al. (1985). Whensonic tracking, the pulse repetition rate of the pres-sure-sensitive sonic transmitter was recorded anddecoded, and the position of the tracking boat, andthe time and depth of the tuna were recordedapproximately every 5 s. Radiotracking receiverswere also mounted on the RV ‘McArthur’ and thepurse seiner. When radio-tracking from any of thevessels, the position, time, heading of the vessel,bearing to the dolphin, and signal strength wererecorded every 15 min. The purse seiner’s helicopterallowed us to observe the be havior of the dolphinsand tuna and monitor changes in herd size andcomposition of the aggregation.
A SEACAT mini-CTD (Sea-Bird model SBE 19) oran ex pendable bathythermograph (XBT) was de -ployed to measure depth and temperature from theRV ‘McArthur’ approximately every 4 h to a depth ofat least 200 m. A shipboard environ-mental data acquisition system(SEAS) collected and processedthese data. Of particular interestwas the correlation of the swimmingdepths of the dolphins and tunawith the depth of the thermocline.
Results
Five dolphins were tracked dur-ing the study from 1 to over 4 d dur-ing 1993 (Scott & Chivers 2009),and 3 focal tuna were tracked for 1,8, and 31 h. Table 1 provides detailsof the capture and tracks madewhen both dolphins and tuna weretagged. These tracks allow us tocompare the horizontal and verticalmovements of the 2 species.
The longest simultaneous trackinvolved Dolphin D8 and Tuna T1.These 2 animals were releasedfrom the net together, along withabout 60 spotted dolphins andabout 100 yellowfin tuna, at 11:20 hon 21 November 1993 (Fig. 1). Thetuna and dolphin separated 2.5 hlater and did not rejoin during therest of the track but remainedwithin 15 n miles of each other. The
tuna came within 400 m of several other dolphinherds the following day, including one herd accom-panied by feeding seabirds, but it did not join theseherds. The dolphin milled over the continental slopeand 15 n miles offshore of the coast over the next 4 d.After excluding the first 2 h of data after release fromthe net, the dolphin’s average travelling speed was9.8 km h−1 (= 6.7 knots [kn] or 2.7 m s−1; Scott &Chivers 2009). The tuna travelled at an averagespeed of 7.4 km h−1 (= 4.6 kn or 2.1 m s−1) along thecontinental slope to the northwest before milling inan area about 15 n miles away from the dolphin.Even though Dolphin D8 and Tuna T1 were sepa-rated for most of their tracks, their diving historieswere recorded simultaneously (Fig. 2).
Dolphin D9 and Tuna T3, along with about 120spotted dolphins and a few tuna, were releasedtogether at 09:46 h on 26 November 1993, but thetuna was tracked for only 1 h due to a malfunction-ing tracking boat. Dolphin D11 and Tuna T5 werecaptured together; D11 was released at 12:45 h on
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Date Position Dolphins Tuna Commentscaptured tagged tagged
19 Nov 17°48’N, 103°30’W D7 (TDR) D7 tracked for 19 h191 cm male
20 Nov 17°21’N, 103°54’W D7 recaptured
21 Nov 18°34’N, 103°57’W D8 (TDR) T1 (V7P) D8 tracked for 49 h198 cm female ~ 25 kg T1 tracked for 31 hwith ~1 yr calf T2 (V3P) T2 not tracked
~ 25 kg
23 Nov 18°37’N, 104°02’W D8 recaptured
26 Nov 18°28’N, 104°14’W D9 (TDR) T3 (V7P) D9 tracked for 102 h196 cm female ~30 kg T3 tracked 1 h
T4 (V3P) T4 not tracked~25 kg
29 Nov 18°23’N, 104°04’W D10 (TDR) D10 tracked 32 h200 cm male
30 Nov 18°21’N, 104°12’W D11 (VHF) T5 (V7P) D11 tracked 11 h175 cm male ~10 kg T5 tracked 8 h
T6 (V3) T6 not tracked~10 kg
30 Nov 18°17’N, 104°16’W Recaptured D9
Table 1. Stenella attenuata and Thunnus albacares. Summary of sets and taggingand tracking operations during 1993. VHF: 148−150 MHz radio transmitteronly; TDR: VHF transmitter plus a time-depth recorder; V7P: 50 kHz pressure-sensitive sonic transmitter; V3P: 60 kHz pressure-sensitive sonic transmitter,
V3: 71 kHz sonic transmitter
Scott et al.: Tuna–dolphin association
30 November (Fig. 1), but T5 could not be backedout of the net with the dolphins and had to bereleased 15 min later. The dolphin was releasedwith 29 spotted and 21 spinner dolphins, and the
tuna was released with about 600 tuna. The tunadid not rejoin the original dolphin herd, but wasclose to a group of dolphins from 19:00 to 22:00 h,as evidenced by the echolocation sounds heardthrough the tracking hydrophone and the visualobservations of rapidly swimming and jumping dol-phins. The tuna’s signal was lost at about 22:00 hwhen the weather worsened and the tuna’s speedincreased. The average speed of Dolphin D11 was9.3 km h−1 (= 5.8 kn or 2.6 m s−1; Scott & Chivers2009) and the average speed of Tuna T5 was 5.1 kmh−1 (= 3.2 kn or 1.4 m s−1). The difference in travel-ling speeds may be due to the relatively small sizeof Tuna T5 (~10 kg) compared to the tuna normallyassociated with dolphins.
The dolphins and tuna showed different swim-ming patterns. The dolphin usually travelled duringthe day at a depth of 15 to 20 m, in the mixed layerabove the thermocline. The characteristics of thedaytime dives (i.e. no rapid ‘wiggles’ or fluctua-tions at depth) suggested the dolphins were notfeeding (Bengtson & Stewart 1992, Testa et al. 1993,Scott & Chivers 2009). The dolphins dove deeper atnight, often below the thermocline, apparently tofeed on organisms associated with the deep scatter-ing layer until dawn (Scott & Chivers 2009). Thedeepest dive was to 121 m.
The tuna showed a different pattern. During theday, the tuna swam in the mixed layer to about thedepth of the thermocline at 35 to 40 m, below thetypical swimming depths of the dolphins. Afterdusk, when the dolphins began to dive deeper, thetuna ascended to depths of about 25 m or less.Near dawn, the 2 species showed strikingly differ-ent changes in swimming depths. As the dolphinsresumed their daytime swimming depth nearer thesurface, the tuna descended toward the thermo-cline. The greatest swimming depth of the tunawas 110 m.
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Fig. 1. Stenella attenuata and Thunnus albacares. (a) Move-ments of Dolphin D8 and Tuna T1 tracked simultaneouslyduring 21 to 23 November 1993 off the Pacific coast of Mex-ico and (b) movements of Tuna T5 and Dolphins D10 andD11 tracked during 29 November to 1 December 1993. T5and D11 were captured together off the Pacific coast of Mex-ico but released 15 min apart; D10 was tagged and releasedthe previous day. Bottom contours shown in meters. Capture
locations are indicated by black circles
Fig. 2. Stenella attenuata and Thunnus albacares. Sample of vertical movements of Tuna T1 (yellow) and Dolphin D8 (orange) simultaneously tracked during 21 to 22 November 1993. The depth of the thermocline is represented as a blue band
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TROPHIC INTERACTIONS
Methods
Stomachs from dolphins and yellowfin tuna weresampled at sea by observers of the Inter-AmericanTropical Tuna Commission (IATTC) during 1992 to1994. The tuna and dolphins were caught by tunapurse-seiners of the international fleet. For dolphinsets in which 3 or more dolphins were sampled (to en-sure a large enough sample size of prey items eatenby the dolphins in that herd), samples were takenfrom up to 25 dolphins and 25 yellowfin tuna. Eachanimal was measured, the sex determined, and thestomach and a core of dorsal muscle were collectedand frozen for food habits and for stable isotope analy-sis (Román-Reyes 2005), respectively. On occasion,the tunas were marked immediately after capture,placed in the vessels’ fish holds, and sampled afterunloading.
In the laboratory, the stomach samples were thawed,and stomach fullness, as a percentage of stomachcapacity, was estimated visually. The stomach con-tents were identified to the lowest taxon possible,weighed, and counted (Galván-Magaña 1999), anddegree of digestion was determined (Olson &Galván-Magaña 2002). The data were stratified by thelocal time of day that the sets began: 06:00−08:59 h,09:00−11:59 h, 12:00−14:59 h, and 15:00−18:00 h.Within each time stratum, the percent occurrence ofprey items that were fresh or in intermediate diges-tion state (‘Recent,’ digestion states 1 and 2 definedby Olson & Galván-Magaña 2002) was calculated.Two stomach fullness strata were calculated for eachtime period. The ‘Full’ category comprised the per-centage of predators whose stomachs were estimatedto be 50 to 100% full of food, and the ‘empty’ cate-gory comprised the percentage of predators that hadempty stomachs or contained only residual hard partsthat could have been consumed on a previous day.
Prey composition in stomach contents was ana-lyzed both by prey weight and prey occurrencebecause these diet indices emphasize different infor-mation about the diet of predators (Chipps & Garvey2007). For each predator species (dolphins or tuna),the proportional composition by weight of each preytype in each individual was computed and averagedfor each prey type over all individuals with foodremains in the stomachs during the entire day, as:
(1)
where MWi is mean proportion by weight for preyitem i, Wij is the weight of prey item i in stomach j, Pis the number of individuals with food in their stom-achs, and Q is the number of prey types in the sample(Chipps & Garvey 2007). Digestion-resistant hardparts (squid mandibles and fish otoliths) were disre-garded to ensure that only recent prey items wereincluded. The occurrence-based prey composition(percentage of all individuals sampled whose stom-achs contained a particular prey species) includedresidual hard parts to provide a longer-term view ofthe diet, although this may include periods of timewhen the tuna and dolphins were not associated. Theprey were grouped into categories according to theirtaxonomy and whether the species remained in theepipelagic zone day and night or migrated verticallyinto the zone at night.
Results
Data were analyzed from the 73 sets that had asample size of at least 3 yellowfin tuna stomachs andat least 3 spotted and/or spinner dolphin stomachs.The 73 sets provided samples from 218 spotted dol-phins, 172 spinner dolphins, and 1523 yellowfin tunathat were spatially distributed across the geographi-cal range of the fishery (Fig. 3). Sets were made dur-ing daylight, with the earliest set at 07:55 h and thelatest set at 18:06 h. Prey remains, excluding residualhard parts, were found in the stomachs of 23% of thespotted dolphins, 17% of the spinner dolphins, and64% of the yellowfin tuna. The principal taxa arelisted in Table 2.
The daily trends in digestion state and stomach full-ness illustrate the difference in the feeding times ofthe dolphins and the tuna (Fig. 4). Most of the spottedand spinner dolphins had full stomachs when caughtduring the early morning, but the percentages withfull stomachs and recently eaten prey de clined andpercentages with empty stomachs in creased through-out the day (Fig. 4). Full stomachs and signs of recentfeeding were rare in the afternoon for both dolphinspecies. The yellowfin tuna, however, showed signs ofrecent feeding and full stomachs throughout the day-time, with the greatest percentage of empty stomachsoccurring in tuna caught in early morning sets(06:00−08:59 h). Thus, the digestion and fullness dataindicate that the dolphins feed mainly at night and inthe early morning, whereas the tuna feed throughoutthe daylight hours but less at night.
Differences in the mass of prey in the stomachsconfirmed that the dolphins fed primarily at night.
MWP
W
Wi
ij
iji
Qj
P
=
⎛
⎝
⎜⎜⎜⎜
⎞
⎠
⎟⎟⎟⎟
=
= ∑∑1
1
1
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The prey weights per stomach sam-pled were (mean ± SE) 29 ± 6 g forspinner dolphins, 101 ± 12 g for spotteddolphins, and 254 ± 11 g for yellowfintuna. The observed prey weights forthe spotted dolphins were only 1 to 8%of what would be expected; an ener-getics study (Edwards 1992) estimatedthat the foraging requirement of spot-ted dolphins is 5 to10 times that of yel-lowfin tuna. This large discrepancybetween the observed prey weightsfor spotted dolphins and that expectedbased on the Edwards energetics modelindicates that daytime sampling under-estimates their prey consumption.
The weight-based measure of preycomposition indicated that spotted dol-phins consumed most of their daily ra-tions during the night and early morning. Forty-threepercent of the food in the stomachs of spotteddolphins during the entire daytime was from animalscaptured between 06:00 and 08:59 h. Prey composi-tion was dominated by vertically migrating cephalo -pods and epipelagic flyingfishes, scombrids, no -meids, and crustaceans (Fig. 5). Spinner dolphinsfed mainly on vertically migrating myctophid fishes(Fig. 5). Daytime feeding by spinner dolphins wasrare; 81% of the food in spinner dolphins’ stomachsduring the entire daytime was from animals capturedbetween 06:00 and 08:59 h. In contrast, yellowfin tunapreyed largely on epipelagic fishes; prey that verti-cally migrates to near-surface waters at night com-prised only minor percentages of the diet. Scombrids,particularly frigate tunas Auxis spp., dominated thefresh food remains during the daytime (Fig. 5).
The occurrence-based measure of prey composi-tion also indicated different feeding times for the dol-phins and tuna. Stomachs from both dolphin specieslargely contained the remains of vertically migratingprey at all times of the day. The vast majority of theseprey remains were digestion-resistant squid man -dibles and fish otoliths, which accumulate in thestomachs. For spotted dolphins, the diurnal patternof prey occurrence supported the weight-based datain that the high prey diversity, which includedepipelagic taxa in the early morning, declined in theafternoon. For spinner dolphins, virtually all occur-rences of cephalopods and fishes in the stomach contents were animals eaten earlier and alreadydigested, with only hard parts remaining. For yellow -fin tuna, epipelagic prey were important in occur-rence throughout the day, although mesopelagic
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Fig. 3. Stenella attenuata, S. longirostris, and Thunnus albacares. Locationswhere stomach samples were collected by IATTC observers aboard purse
seiners during 1992 to 1994
Category Order (O) or Family (F) Species Common name Predator
Vertical migratingCephalopods Ommastrephidae (F) Dosidicus gigas Jumbo or Humboldt squid Ta, SaFishes Phosichthyidae (F) Vinciguerria lucetia Lightfish Ta, Sl
EpipelagicCephalopods Teuthoidea (O) Thysanoteuthis rhombus Diamondback squid Ta
Argonautidae (F) Argonauta spp. Argonauts TaExocoetids Hemiramphidae (F) Oxyporhamphus micropterus Bigwing halfbeak Ta, Sa
Exocoetidae (F) Exocoetus volitans Tropical two-wing flyingfish Sa, TaScombrids Scombridae (F) Auxis spp. Frigate and bullet tunas Sa, TaNomeids Nomeidae (F) Cubiceps pauciradiatus Driftfish Ta, Sl, SaOther epipelagic fishes Ostraciidae (F) Lactoria diaphanum Boxfish TaCrustaceans Galatheidae (F) Pleuroncodes planipes Pelagic red crabs Ta
Portunidae (F) Euphylax robustus Swimming crabs Ta
Table 2. Stenella attenuata, S. longirostris, and Thunnus albacares. Categories of prey remains in the stomach contents of spot-ted dolphins (Sa), spinner dolphins (Sl), and yellowfin tuna (Ta), and the principal prey based on percent mass in each category
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Fig. 4. Stenella attenuata, S. longirostris, and Thunnus al-bacares. Percentages of predators whose stomachs were es-timated to be 50 to 100% full (‘Full’) and stomachs that hadno fresh remains (‘Empty’), and percent occurrence of allprey items, including residual hard parts, in digestion states1 and 2 (‘Recent’). The data were stratified by time ofday that the sets were initiated: 06:00−08:59 h (10 sets),09:00−11:59 h (14 sets), 12:00−14:59 h (28 sets), and15:00−18:00 h (21 sets). The sum of the percentages of Fulland Empty stomachs is less than 100% because those with
fullness >0 to 49% are not displayed
Fig. 5. Stenella attenuata, S. longirostris, and Thunnus al-bacares. Percentage composition by weight (see Eq. 1) ofeach prey type in each individual tuna or dolphin averagedfor each prey type over all tuna or dolphins with food re-mains in the stomachs during the daytime (06:00−18:00 h).Error bars are 2 SE from the mean. The data for residual
hard parts were omitted
Scott et al.: Tuna–dolphin association
cephalopods were also high in occurrence during thedaytime after 09:00 h, which is likely due to residualmandible retention (81 to 94% of the records werehard parts).
SPATIAL ASSOCIATIONS
Methods
IATTC or national observer programs have moni-tored virtually 100% of the large tuna purse-seinersfishing in the ETP since 1992. These observers collectinformation on dolphin sightings, tuna catches, mor-talities of dolphin and other bycatch species, andother data (Bayliff 2001). Dolphin sighting and dol-phin set data from 1995 to 2005 were stratified by 5°quadrat for pure herds of spotted and spinner dol-phins and mixed-species herds of these 2 species.Data were included only if the purse-seiner hadmade at least one dolphin set during the cruise. Thedata base included trips monitored by observers fromthe IATTC (all years) and the national programs ofVenezuela (2000 to 2005), Ecuador (2001 to 2005),and Colombia (2005). Data from the Mexican na -tional program that monitors half of the Mexican fleetwere, however, not available for this study.
The percentage of sets-to-sightings was used as anindex of the prevalence of the tuna-dolphin asso -ciation. Sightings included those made and identifiedas pure and mixed herds of offshore spotted andspinner dolphins by either the observer, or the ship-board or helicopter crew members.
Because data requiring identification of dolphinspecies by crew members were used in these calcula-tions, only the 2 species that the crews were mostfamiliar with, spotted and spinner dolphin, were con-sidered. There are also caveats about the use of theindex. The index likely overestimates the prevalenceof the association because some dolphin sightings bythe crew may not have been reported to the observerwhen no tuna were present, and this bias may haveincreased somewhat since the 1980s (Lennert-Codyet al. 2001). Another potential cause of overestima-tion is that small herds of dolphins are less likely tobe detected and less likely to carry tuna than largerherds. However, we found no significant inter-annual differences in the index for the 1995 to 2005time period chosen. We included only those quadratswhere sightings of either of the 2 dolphin specieswere recorded by the purse-seiner observers, indi-cating that the quadrat was within the distributionalranges of both the dolphins and fishery.
Using a linear regression, the tuna-dolphin asso -ciation index for each 5° quadrat was modeled as afunction of the 1995 to 2005 average mixed-layerdepth for the corresponding quadrat. The mixed layerdepth (the depth at which temperature equals the seasurface temperature minus 0.8°C) was calculatedfrom the Simple Ocean Data Assimilation model(Carton et al. 2000) and served as a proxy for both thedepth of the thermocline and the upper boundary ofthe oxygen minimum zone. The annual averagemixed-layer depth was used for most quadrats, butfor some quadrats, where the fishery only occurredin a few months of the year, 1 or 2 quarterly averageswere used instead to match the months in which thedolphin sightings were recorded.
Results
The percentage of single-species sightings that ledto sets (indicating tuna were likely present) was 42%for spotted dolphins (39 593 sets in 94 202 sightings);the percentage ranged as high as 73% but declinedto less than 30% where the mixed layer depth deep-ened to over 40 m. The average for spinner dolphinswas only 20% (3159 sets in 15 888 sightings); the per-centage ranged as high as 46% but declined to 15%or less where the mixed layer depth deepened toover 30 m. Mixed herds of spotted and spinner dol-phins had the highest percentage with 54% (32 094sets in 59 778 sightings). The higher percentage formixed herds is likely due to these herds tending to belarger than single-species herds and larger herdstending to be more attractive to fishermen becausethey yield larger catches of yellowfin tuna (Scott &Cattanach 1998, Perkins & Edwards 1999).
The mixed layer is very shallow in the eastern trop-ical Pacific, but deepens to the west (Fig. 6). A linearregression of the association index on mixed layerdepth showed significant trends for pure herds ofspotted (p < 0.01) and spinner dolphins (p < 0.01), andfor mixed spotted-spinner dolphin herds (p = 0.01).The association between tuna and dolphins increasedas the mixed-layer depth shallowed.
For spotted dolphins, the association is most preva-lent in waters where the depth of the mixed layer isabout 45 m or less (Figs. 6 & 7), and the oxygen con-centration below the mixed layer is extremely low.The spatial pattern of mixed spotted-spinner herdswas similar to that of spotted dolphins. Pure spinnerdolphin herds are not thought to normally carry tuna(unless spotted dolphins are also present). However,there are areas where the association with tuna is
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relatively strong—areas where the depth of the mixedlayer is about 25 m or less (Figs. 6 & 8), with a hypoxicoxygen minimum zone below.
Distribution plots of sets on tuna associated withspotted and spinner dolphins show that the spatialextent of the tuna–dolphin association changes sea-sonally. For the spotted dolphin, there are areasalong the northern and southern margins of the dis-tribution where the association is prevalent only inthe summer (Fig. 7), while for the spinner dolphin, asouthern cluster of sets is present only in the australsummer (Fig. 8). This expansion in the distribution ofdolphin sets coincides with the summer shallowing ofthe mixed layer, particularly north of 20° N and southof 15° S (Fiedler 1992). This seasonal pattern is illus-trated in a 5° quadrat (85 to 90°W, 10 to 15°S) wherethe seasonal differences in dolphin sets were partic-ularly dramatic; sets occurred only when the averagedepth of the mixed layer was at a minimum (Fig. 9).
DISCUSSION
Tunas are known to associate often with floatingobjects, whale sharks, whales, and dolphins (see re-views in Scott et al. 1999). In the ETP, small tunas arecommercially caught in association with floating ob-jects or as free-swimming (unassociated) schools, butlarge yellowfin tuna are usually caught in associationwith dolphins. A ‘meeting place’ hypothesis has beenproposed that links the associations of small tunasand floating objects and large yellowfin tuna withdolphins by arguing that tunas have a genetic predis-
position to associate with objects. Thiscould serve as a mechanism to increasetheir own encounter rates and facilitateschool formation (Fréon & Misund1999, Fréon & Da gorn 2000). These au-thors have suggested that tuna–dol-phin aggregations may represent aspecific version of the ‘meeting point’phenomenon whereby the dolphinschool, while mobile, provides a cuethat allows yellowfin tuna to aggregateinto larger schools.
Two main hypotheses to explain whytuna and dolphins associate propose (1)benefits due to increased foraging effi-ciency, or (2) benefits from reduced riskof predation. To fully explain the asso-ciation we must determine which spe-cies initiates the association andwhether the association is obligatory or
facultative for one or both species. The hypothesismust explain not only the benefits of the association,but why yellowfin tuna associate primarily with spot-ted dolphins, to a lesser extent with spinner dolphinsand common dolphins, and rarely, if ever, with theseveral other species of dolphins occurring in the ETP;why this association involves primarily large yellowfintuna and not small yellowfin or other tunas; and whydolphins and tuna associate in the ETP and only to amuch a lesser degree, if at all, in other oceans.
Which species follows the other?
This is not as simple a question as it may appearbecause there are no obvious ‘leaders’ or ‘followers’in the spatial sense—one species or one individual isnot always in front of the aggregation and the speciesthat initiates the association may not be obvious. Inthe constantly shifting aggregations of tuna and dol-phins, individuals or species in front of the aggrega-tion at one moment will find themselves on the flankor rear of the aggregation when it changes direction.Early observations by baitboat fishermen (Silva 1941)suggested the tuna followed the dolphins, but others(Godsil 1938) suggested the opposite. Most fisher-men, however, have come to believe that the tunafollow the dolphins (National Research Council 1992,Felando & Medina 2011). They consistently observedthat if the dolphins moved away from the baitboat,the tuna would follow, even while the fishermenwere chumming the water with live baitfish. Whenthe purse-seine fishery began, the fishermen ob -
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Fig. 6. Average annual mixed layer depths (in m) during 1995 to 2005 (adaptedfrom Fiedler & Talley 2006). Note that the depth of the mixed layer, represent-ing the top of the thermocline, is shallowest (blue) in the eastern tropical Pacific
and deepens to the west (yellow)
Scott et al.: Tuna–dolphin association
served that successfully herding the more-visibledolphins reliably yielded catches of tuna, whereaswhen even a small part of the dolphin herd escaped,the tuna often followed them out of the net andescaped as well (National Research Council 1992).
Researchers have also proposed different ideasabout which species initiates the association. Au &Pitman (1986, 1988) suggested that the tunas’ abilityto drive prey to the surface attracts seabirds andcould attract the behaviorally adaptable dolphins aswell, while Norris et al. (1994) argued that it would beadvantageous for the tuna to exploit the dolphins’
ability to echolocate and find preypatches at a distance. Scientists ob-serving underwater behavior insidethe purse-seine net suggested that thetuna follow dolphins (Norris et al.1978, Pryor & Kang 1980). Mathemati-cal population models have indicatedthat the species with the shorter life -span, the tuna, must benefit if the asso-ciation is to re main stable (Mullen1984). Comparative bio energetics mod-els suggested that it is unlikely thatdolphins initiate the association be-cause the dolphins have greater forag-ing requirements (Edwards 1992).
Is the association obligatory orfacultative?
Yellowfin tuna and spotted dolphinsare both found throughout the tropicsbut only have a persistent, spatially ex-tensive association in the ETP, so it isnot likely that the association is ob -ligatory for either species. The trackingresults supported this: even thoughTuna T1 and Dolphin D8 were caughtand released together, they separatedshortly afterwards and T1 did not joinother dolphin herds that were sightedabout 400 m away. A previous trackingstudy of yellowfin tuna in the ETP alsoshowed that tagged tuna sometimesjoined nearby herds of spotted dolphinsand at other times did not (Carey & Ol-son 1982). A study of dolphin and tunagroup sizes found that spotted andspinner dolphin herds and yellowfintuna schools all increased in numbersduring the day and fragmented at
night (Scott & Cattanach 1998). The nighttime frag-mentation of both dolphin and tuna aggregations ledthe authors to suggest that the tuna–dolphin associa-tion weakened at night as well.
What are the benefits of the tuna–dolphin association?
In the light of the results of our 3 studies, we re-examine the 2 hypotheses put forward previously.It has often been suggested that there is not a
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Fig. 7. Stenella attenuata and Thunnus albacares. Sets on tuna associated withpure herds of spotted dolphins from 1995 to 2005 during April to September
and October to March
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single cause for the tuna–dolphin association, butrather a combination of factors (Hammond 1981,Au & Pitman 1988, Scott & Cattanach 1998, Fréon& Dagorn 2000). As with conspecific schools, thesize of a mixed-species group is likely a result ofthe dynamic balance between the risk of predationtending to increase group size for protection, andprey dis tribution tending to limit groups to a sizethat can be sustained by the available resources(Jarman 1974, Janson & Goldsmith 1995, Scott &Cattanach 1998).
Foraging benefits
The results of Perrin et al.’s (1973)food-habits study not only indicatedthat there was overlap in the prey spe-cies eaten by spotted dolphins and yel-lowfin tuna, but provided evidence ofprey species specialization as well. Spot-ted dolphins and yellowfin tuna werethought to feed primarily on epipelagicprey, while spinner dolphins fed pri-marily on meso pelagic prey (see alsoFitch & Brownell 1968, Morán-Anguloet al. 1995). The observation that tunaassociate more readily with spotteddolphins than with spinner dolphinsled other authors to suggest that thesimilarity in food habits is the basis ofthe tuna-dolphin association and thatone or both of the species gains feed-ing benefits from the association (Norris1978, Norris & Dohl 1980a, Au & Pitman1986, 1988, Pryor & Kang-Schallen-berger 1991, Au 1991, Edwards 1992,Norris et al. 1994). However, the sam-ple size (5 sets from which both dol-phin and tuna stomachs were exam-ined) in Perrin et al.’s (1973) study wastoo small to detect feeding differencesbetween yellowfin tuna and spotteddolphins by time of the day.
Food habits data collected in ourstudy from 73 sets in which tuna anddolphins were caught together do notsupport the feeding hypothesis. Thetuna–dolphin association is primarily adiurnal one (Scott & Catta nach 1998)and if the association was based onfeeding benefits, one would expectboth dolphins and tuna to feed primar-ily in the daytime. In the ETP, how-ever, yellowfin tuna are primarily day-
time feeders, while spotted and spinner dolphins areprimarily nighttime or crepuscular feeders (Reintjes& King 1953, Alverson 1963, Shomura & Hida 1965,Fitch & Brownell 1968, Perrin et al. 1973, Ortega-García et al. 1992, Buckley & Miller 1994, Perrin& Hohn 1994, Richard & Barbeau 1994, Roger 1994,Robertson & Chivers 1997, Fiedler et al. 1998, Scott &Cattanach 1998, Galván-Magaña 1999, Román-Reyes 2005, this study). While yellowfin tuna mayalso feed at night and both dolphin species feed occa-sionally during the day, daytime feeding is clearly
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Fig. 8. Stenella longirostris and Thunnus albacares. Sets on tuna associatedwith pure herds of spinner dolphins from 1995 to 2005 during April to
September and October to March
Scott et al.: Tuna–dolphin association
more important for the tuna and nighttime feeding ismore important for the dolphins.
The food-habits study found that, while there issome overlap in the diets of spotted dolphins and yellowfin tuna, the prey resources were largely parti-tioned by time of day, prey species, and size (Galván-Magaña 1999). Stable isotope analysis performed onmuscle samples from a subset of the predators ana-lyzed for food habits (Román-Reyes 2005) revealedtrophic overlaps of about 78% between yellowfin andspotted dolphins and between spotted and spinnerdolphins, but only 57% between yellowfin and spin-ner dolphins. Despite similarity among δ15N values ofthe predators, trophic-level overlap only requires feed-ing on prey from overlapping trophic levels, and canoccur without sharing any of the same prey species.The tracking data also suggested that the yellowfintuna and spotted dolphins feed at different depths.
Although the hypothesis that the association is largelyfood-based is not supported by current evidence,there may still be a foraging benefit. Both dolphin andtuna groups disaggregate during the night, beginningat dusk when dolphins begin to feed (Scott & Catta -nach 1998, Scott & Chivers 2009). The feeding times ofthe spotted dolphins and yellowfin tuna overlap in thedawn hours, however, and early morning feeding boutson multi-species concentrations of prey may draw tunas,dolphins, and other predators into proximity, and thusserve as a catalyst in the creation of the association.
Protection from predators
Travelling in groups provides more protection frompredation than travelling alone. This advantage can
extend to multi-species aggregations,whereby the combined number of indi-viduals of all species dilutes the risk ofpredation to individuals. Mixed-speciesaggregations comprised of differentspe cies with different sensory capabili-ties may also detect predators moreefficiently than either species couldprovide alone (e.g. Diamond 1988).
Spotted dolphins and yellowfin tunaare of a similar size and have the samepotential predators (Scott & Cattanach1998). The predation risk may be partic-ularly high for the yellowfin tuna be-cause sharks and billfishes are signifi-cant predators that are commonly caughtwith tunas (Au 1991, Hunsicker et al.2012). Hunsicker et al. (2012) found that
even large yellow fin tuna were prey for large sharks,particularly in the ETP, and they suggested that yellowfin tuna should more properly be considered amesopredator rather than an apex predator.
Rare observations of shark attacks on spotted dol-phins illustrate how vulnerable dolphins may bewhen the protection provided by being part of a herdis disrupted. Leatherwood et al. (1973) reported ob -servations of shark predation on spotted dolphinsafter the herd’s structure had been disrupted by fish-ing operations in the ETP. Maldini’s (1993) observa-tion of an attack of a tiger shark Galeocerdo cuvier ona juvenile spotted dolphin off Hawaii illustrated thehigh predation risk faced by calves and juveniles andthe vulnerability of dolphins when they stray outsidethe envelope of the herd. Successful attacks bysharks were typically ambushes initiated from behindand below the dolphin.
Our results are in line with the expectations of the‘meeting point’ hypothesis proposed to explain theschooling of pelagic tunas (Fréon & Misund 1999,Fréon & Dagorn 2000). The mobile dolphin herdsmay serve as a cue that allows tunas to aggregateinto larger schools. At the same time, the benefit of‘safety in numbers’ is accentuated by the combinedgroup size of 2 or more similarly sized species. Scott& Cattanach (1998) noted that predation pressureneed not be high to promote these aggregations, onlythat the risk of predation should be less than thatincurred by an alternate strategy, such as formingsmall groups or straying from the group in the pres-ence of predators.
Large sharks are not only potential predators, butcompetitors as well (Leatherwood et al. 1973, Com-pagne 1984, Heithaus 2001, Acevedo-Gutiérrez 2002,
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Fig. 9. Stenella attenuata, S. longirostris, and Thunnus albacares. Number ofsets from 1995 to 2005 made on tuna associated with pure herds of spottedand spinner dolphins by month in one 5° quadrat (85 to 90° W, 10 to 15° S).Overlaid is the average mixed layer depth for that same quadrat by month
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Maldini 2003). Pelagic sharks would be attracted tothe same prey patches as the dolphins and tuna, andhabitat compression would likely increase theirencounters. By monitoring each others’ alarm re -sponses, the dolphins and tuna could both gain fromthe association. The dolphins can echolocate or hearpredators at a distance, allowing them, and the asso-ciated tuna, to avoid or monitor the predators.Because dolphins are most vulnerable to sharkattacks coming from behind and below (Cockcroft etal. 1989, Mead & Potter 1990, Scott & Cattanach1998), any alarm responses by deeper-swimmingtuna could alert the dolphins to predators beneaththem. Similarly, the surface-swimming spinner dol-phins, which have been hypothesized to seek outspotted dolphin herds to increase protection frompredation (Norris 1978, Norris & Dohl 1980b, Norriset al. 1994, Cramer et al. 2008, Kiszka et al. 2011),could also be alerted by the deeper-swimming spot-ted dolphins (discussed below).
Why does this association primarily involve spotteddolphins, much more so than other dolphin species?
If the predation hypothesis is valid, it would re -quire an explanation for why, if tuna join dolphinherds seeking safety in numbers, do they associatemainly with spotted dolphins, even though other spe-cies, particularly spinner and common dolphins, formlarge herds that would provide protection as well.
The weaker association between yellowfin tunaand common dolphins can be explained by their different habitats. Yellowfin tuna are found primarilyin tropical waters, while common dolphins tend toinhabit cooler, upwelling-modified waters (Au & Per-ryman 1985, Reilly 1990, Fiedler & Reilly 1994, Reilly& Fiedler 1994, Ballance et al. 2006).
Spinner dolphins, however, inhabit tropical watersand associate with yellowfin tuna, but generally aspart of a mixed-species spotted-spinner dolphin herd.Spotted and spinner dolphin herds coalesce through-out the mornings such that, by mid-day, 87% of allspinner dolphin sightings are in mixed-species herdsassociated with spotted dolphins (Scott & Cattanach1998). The apparent weaker association between yel-lowfin tuna and spinner dolphins may be explained,in part, because tuna encounter pure spotted dolphinherds and mixed spotted-spinner dolphin herds morefrequently than pure spinner dolphin herds. Thus,even when tuna join pure spinner dolphin herds inthe early morning, it is likely that those herds willsoon coalesce with herds of spotted dolphins.
The tuna’s apparent preference for spotted dol-phins can also be explained by their swimmingdepths. The foraging depths of yellowfin tuna arerestricted by low dissolved oxygen concentrations,and they cannot swim for long in waters where theconcentrations are less than 2.0 ml l−1 without resort-ing to ‘bounce diving’ (Schaefer et al. 2009). Trackingstudies (Carey & Olson 1982, Holland et al. 1990,Block et al. 1997, Schaefer et al. 2007, 2009, thisstudy) have shown that yellowfin tuna are typicallyfound during the daytime near or slightly above thethermocline (20 to 60 m deep in the ETP areas wherethe association is most often observed and exploitedby the fishermen). Aerial photogrammetry studieshave observed that spinner dolphins are easier tophotograph than spotted dolphins (Cramer et al.2008) because spinner dolphins swim near the sur-face while spotted dolphins swim deeper (W. Perry-man & M. D. Scott pers. obs.); the TDR data confirmedthat the spotted dolphins swim at depth, travelling 15to 20 m below the surface during the daytime. Radio-tracking and aerial photo grammetry data also indi-cate that common dolphins, like spinner dolphins,are also surface swimmers during the day (Evans1974, W. Perryman & M. D. Scott pers. obs.). Thus,the depth at which spotted dolphins typically swim ismuch closer to the typical swimming depth of the yel-lowfin tuna than that of the spinner and common dol-phins. It would be easier for the tuna, swimming justabove the thermocline, to maintain an associationwith the deeper-swimming spotted dolphins than the surface-swimming spinner dolphins.
If differences in swimming depth were indeed in -fluencing the formation of the tuna–dolphin asso -ciation, then one might expect tuna to associate withspinner dolphins where the mixed layer was the shallowest and the oxygen minimum zone just belowthe mixed layer was most hypoxic. Comparison of themixed layer depth (Fig. 6) to the distribution of setson tuna associated with pure herds of spinner dol-phins (Fig. 8) and with spinner dolphins in southernareas during summer when the mixed layer depth isshallower (Fig. 9) suggests that this is so.
Why does this association involve primarily largeand not small tunas?
The yellowfin tuna caught by purse seines in asso-ciation with floating-object sets are small (averaging2.6 to 4.6 kg, modal fork length [FL] ~45 cm, depend-ing on area), those caught in unassociated schoolsare larger (8.7 to 11.2 kg, modal FL ~70 cm), and
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those caught in association with dolphins are thelargest (13.5 to 37.3 kg, modal FLs >90 cm; IATTC2004). Edwards (1992) argued that it would not beenergetically efficient for small yellowfin tuna orskipjack to travel with dolphins until they reached atleast the same length of a newborn spotted dolphin(about 85 cm, Hohn & Hammond 1985; or a weight ofabout 12.9 kg, Wild 1986). Otherwise, Edwards (1992)argues, smaller tunas would have to travel faster thantheir optimum cruising speed to keep up with thedolphins, which is energetically unsustainable. Whensmall tunas are associated with dolphins, they docomprise a small proportion of the catch, likely be -cause they may not be able to keep pace during thehigh-speed chase that usually precedes a dolphin set.
Why is the association of dolphins and tuna such apredominant feature in the ETP, but not in most
other oceans?
It has long been suggested that the unusualoceanographic features of the ETP—the high surfacetemperatures, shallow thermocline (<60 m deep),and the thick oxygen minimum zone—promotes theassociation of tuna and dolphins (Green 1967, Perrinet al. 1976, Au & Perryman 1985, Edwards 1992, Nor-ris et al. 1994). Oxygen is depleted in warm waters ofthe mixed layer due to high phytoplankton produc-tion, and the stable thermocline prevents oxygena-tion of the cooler waters below, producing the char-acteristic thick oxygen minimum zone (see review byFiedler & Talley 2006). The oxygen minimum zone inthe ETP ‘includes a greater body of almost oxygen-free water than any other region in the world’soceans’ (Knauss 1963). To the west, the thermoclinedeepens to about 150 m and the oxygen minimumzone thins markedly (Knauss 1963, Sprintall &Cronin 2001, Tomczak 2001), and the tuna–dolphinassociation becomes uncommon. Tuna purse seinersin the western Pacific rarely set on dolphins (Don-ahue & Edwards 1996, Hall 1998, Hampton & Bailey1999, WCPFC 2011).
The combination of a shallow thermocline and athick layer of cold hypoxic water just below isthought to restrict the vertical movements of tunas(Edwards 1992, Brill 1994, Prince & Goodyear 2006).Although yellowfin tuna may make occasional divesdown into very cold water (Carey & Olson 1982,Block et al. 1997, Dagorn et al. 2006), their verticalrange appears to be limited by temperatures that areabout 8°C less than the surface temperatures (Brill &Lutcavage 2001) and by an oxygen content of about
3.5 ml l−1 or 152 µmol kg−1 (Cayré 1991, Cayré andMarsac 1993, Brill 1994, Graham & Dickson 2004,Prince & Goodyear 2006).
This compresses the yellowfin tuna habitat to thesurface waters of the mixed layer and allows thetuna–dolphin association to occur. Yellowfin tunatend to swim just above the thermocline, with fre-quent excursions upward within the mixed layer(Carey & Olson 1982, Holland et al. 1990, Block et al.1997, Brill et al. 1999, this study); the air-breathingspotted dolphins are obviously tied to the surface,and spend most of their time in the mixed layer trav-elling and foraging. The shallow thermocline alsopromotes propagation of dolphin sounds, and yel-lowfin tuna may detect these sounds at distances ofseveral hundred meters (Finneran et al. 2000, Schae-fer & Oliver 2000). The deeper the thermocline, how-ever, the greater the vertical distance there isbetween the 2 species, and the more difficult it wouldbe to maintain the association. This would explainwhy the association is so prevalent in the ETP andthen becomes progressively rarer farther to the west.It may also explain the effects on tuna catches duringsome El Niño years. During the severe 1983 El Niño,for example, the mixed layer in the ETP deepenedover a wide area, and likely as a result, made thetuna–dolphin association more difficult to maintain,which likely explains the greatly reduced number ofdolphin sets and tuna catches in that year (Fig. B-4 inIATTC 2004).
The association between dolphins and tuna is notentirely unique to the ETP, however. Tuna associatewith dolphins around many islands: the Maldives(Anderson & Shaan 1999), Sri Lanka (de Silva & Boni-face 1991, Leatherwood & Reeves 1991), Fernandode Noronha Archipelago (Sazima et al. 2006), theAzores (Clua & Grosvalet 2001, Silva et al. 2002),Hawaii (Shallenberger 1981), and the Philippines,Indonesia, and New Guinea (Dolar 1994, Hampton &Bailey 1999, WCPFC 2011). These associations maybe promoted by the shallower thermocline in the leeof some islands (e.g. McManus et al. 2008). Dolphinsand tuna are also known to associate, to a muchlesser extent than in the ETP, in the tropical waters ofthe western Indian and the eastern Atlantic Oceans(Simmons 1968, Levenez et al. 1980, Pereira 1985,Donahue & Edwards 1996, Ballance & Pitman 1998,Hall 1998, Ariz-Telleria et al. 1999, Van Waerebeeket al. 1999, Felando & Medina 2011). These oceanregions contain areas with a shallow thermocline anda marked oxygen minimum zone (Fig. 10), althoughthese areas are not as expansive nor is the oxygenminimum zone as hypoxic as in the ETP (Tomczak
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2001, Prince & Goodyear 2006, Prince et al. 2010).Only in the ETP is the association strong enough andreliable enough for a pelagic commercial purse-seinefishery to take advantage of the association consis-tently (Donahue & Edwards 1996, Hall 1998, Scott etal. 1999).
CONCLUSIONS
The ‘meeting point’ hypothesis (Fréon & Misund1999, Fréon & Dagorn 2000) proposes that tuna havea genetic tendency to associate with floating objects,dolphins, whales, or whale sharks. Observations byfishermen and studies by researchers have providedevidence that it is the yellowfin tuna that initiates theassociation with dolphins. Our results, however, sug-gest that the tuna–dolphin association is neither anobligatory nor a permanent one. It involves mainlylarge yellowfin tuna, and not small yellowfin or skip-jack tunas, likely due to energetic constraints onsmall tunas (Edwards 1992). It involves mainly spot-ted dolphins, and only to a lesser extent other dolphinspecies, due to the closer match in habitat and travel-ling depths of the spotted dolphins with the yellowfintuna. The association is most common in the ETPbecause this large region is characterized by warmwaters and a shallow thermocline overlaying a thick
hypoxic oxygen minimum zone that compresses thehabitat for the tuna (Prince & Goodyear 2006). Theshallower the thermocline and the more hypoxic thewaters below the thermocline, the more likely it isthat the association will occur.
The results of our studies support the hypothesisthat the formation of large, mixed-species groups ofspotted dolphins and yellowfin tuna reduces the riskof predation for one or both species. Both speciesshow increased group sizes during the day, likely forthe same reason, as both are potential prey for largesharks and small whales (Scott & Cattanach 1998).The habitat compression that promotes the tuna–dolphin association may also increase the number ofencounters with sharks. Large sharks are both poten-tial predators on and competitors with dolphins andtuna. All of these species are likely attracted to thesame prey patches, particularly during early morningfeeding bouts. The dolphin–tuna association maythen be maintained throughout the day because ofthe threat sharks pose as potential predators.
Acknowledgements. This research has been based on a sci-entific foundation built by many people, over many decades,and covering many disciplines. Many of the insights in thisstudy were influenced by the observations of fishermen andthe research of R. Allen, D. Au, R. Brill, L. Dagorn, E.Edwards, F. Galván-Magaña, M. Hall, P. Hammond, A.Hohn, K. Norris, E. Prince and P. Goodyear, S. Reilly, W. Per-
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Fig. 10. Global minimum dissolved oxygen concentration (µmol kg–1) from World Ocean Atlas 2001 (adapted from Fiedler &Talley 2006). Letters indicate approximate areas where published accounts refer to a tuna–dolphin association: (A) Gulf ofOman and Arabian Sea: Van Waerebeek et al. (1999), Ballance & Pitman (1998); (B) Sri Lanka: de Silva & Boniface (1991),Leatherwood & Reeves (1991); (C) Archipelagic waters of Indonesia, Philippines, and New Guinea: Dolar (1994), Hampton& Bailey (1999), WCPFC (2011); (D) Hawaiian Islands: Shallenberger (1981); (E) Eastern tropical Pacific: Figs. 7 & 8; (F) Fernando de Noronha archipelago: Sazima et al. (2006); (G) Azores Islands: Clua & Grosvalet (2001), Silva et al. (2002);
(H) Gulf of Guinea: Simmons (1968), Levenez et al. (1980)
Scott et al.: Tuna–dolphin association
rin and his many colleagues, and W. Stuntz. Many of thesecolleagues have sharpened our ideas during many discus-sions over the years. Commander D. Peterson and the crewof the RV ‘McArthur’ provided support, advice, and encour-agement to safely conduct our tagging and tracking opera-tions. The crew integrated themselves into every facet of theresearch: tagging and tracking dolphins and tuna, logisticalsupport, scientist-overboard recovery, and collecting envi-ronmental data. The purse seiner ‘Convemar’ was charteredby the IATTC and the Programa Nacional para el Aprove -cha mi ento del Atún y Protección de los Delfines of Mexico.Captain B. Cervantes and the crew of the ‘Convemar’helped in the safe capture, release, and tracking of the dol-phins and tuna. We thank the small army of people from theIATTC, NMFS, and NOAA Corps who supported the projectlogistically. We also thank the biologists who accompaniedus in the field: G. Aldana, W. Armstrong, J. Asch, D. Bratten,M. García, J. Ramírez, H. Rhinehart, and B. Wetherbee. Thestomach and muscle-tissue samples were collected byIATTC observers, and the stomach contents were processedby F. Galván-Magaña and J. Martinez. The stable isotopesamples were analyzed by J. Román-Reyes. We thank themand the many IATTC staff members who participated in thetraining and logistics of the trophic relations study. The datafor the spatial study of the fishery were collected by ob -servers of the IATTC and of national programs, N. Vogelperformed the ‘data extraction from Hell’ to assist in theanalyses, and R. Allen and C. Patnode created the illustra-tions. The manuscript was reviewed by B. Bayliff, R. Deriso,C. Lennert-Cody, W. Perrin, W. Perryman, G. Watters, and 3anonymous reviewers.
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